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Differential cortical layer engagement during seizure initiation and spread in humans

Author

Listed:
  • Pierre Bourdillon

    (Massachusetts General Hospital and Harvard Medical School
    Hospital Foundation Adolphe de Rothschild
    Paris Cité University)

  • Liankun Ren

    (Capital Medical University
    Chinese Institute for Brain Research)

  • Mila Halgren

    (Massachusetts Institute of Technology)

  • Angelique C. Paulk

    (Massachusetts General Hospital and Harvard Medical School)

  • Pariya Salami

    (Massachusetts General Hospital and Harvard Medical School)

  • István Ulbert

    (Institute of Cognitive Neuroscience and Psychology
    Péter Pázmány Catholic University
    Semmelweis University)

  • Dániel Fabó

    (Semmelweis University)

  • Jean-Rémi King

    (PSL University, CNRS)

  • Kane M. Sjoberg

    (Massachusetts General Hospital and Harvard Medical School
    Harvard College)

  • Emad N. Eskandar

    (Albert Einstein College of Medicine – Montefiore Medical Center)

  • Joseph R. Madsen

    (Harvard Medical School)

  • Eric Halgren

    (University of California, San Diego)

  • Sydney S. Cash

    (Massachusetts General Hospital and Harvard Medical School)

Abstract

Despite decades of research, we still do not understand how spontaneous human seizures start and spread – especially at the level of neuronal microcircuits. In this study, we used laminar arrays of micro-electrodes to simultaneously record the local field potentials and multi-unit neural activities across the six layers of the neocortex during focal seizures in humans. We found that, within the ictal onset zone, the discharges generated during a seizure consisted of current sinks and sources only within the infra-granular and granular layers. Outside of the seizure onset zone, ictal discharges reflected current flow in the supra-granular layers. Interestingly, these patterns of current flow evolved during the course of the seizure – especially outside the seizure onset zone where superficial sinks and sources extended into the deeper layers. Based on these observations, a framework describing cortical-cortical dynamics of seizures is proposed with implications for seizure localization, surgical targeting, and neuromodulation techniques to block the generation and propagation of seizures.

Suggested Citation

  • Pierre Bourdillon & Liankun Ren & Mila Halgren & Angelique C. Paulk & Pariya Salami & István Ulbert & Dániel Fabó & Jean-Rémi King & Kane M. Sjoberg & Emad N. Eskandar & Joseph R. Madsen & Eric Halgre, 2024. "Differential cortical layer engagement during seizure initiation and spread in humans," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48746-8
    DOI: 10.1038/s41467-024-48746-8
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    References listed on IDEAS

    as
    1. Elliot H. Smith & Jyun-you Liou & Tyler S. Davis & Edward M. Merricks & Spencer S. Kellis & Shennan A. Weiss & Bradley Greger & Paul A. House & Guy M. McKhann II & Robert R. Goodman & Ronald G. Emerso, 2016. "The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
    2. Catherine A. Schevon & Shennan A. Weiss & Guy McKhann & Robert R. Goodman & Rafael Yuste & Ronald G. Emerson & Andrew J. Trevelyan, 2012. "Evidence of an inhibitory restraint of seizure activity in humans," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
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